Ultra high-resolution biomechanics suggest that substructures within insect mechanosensors decisively affect their sensitivity

Abstract

Insect load sensors, called campaniform sensilla (CS), measure strain changes within the cuticle of appendages. This mechanotransduction provides the neuromuscular system with feedback for posture and locomotion. Owing to their diverse morphology and arrangement, CS can encode different strain directions. We used nano-computed tomography and finite-element analysis to investigate how different CS morphologies within one location—the femoral CS field of the leg in the fruit fly Drosophila —interact under load. By investigating the influence of CS substructures' material properties during simulated limb displacement with naturalistic forces, we could show that CS substructures (i.e. socket and collar) influence strain distribution throughout the whole CS field. Altered socket and collar elastic moduli resulted in 5% relative differences in displacement, and the artificial removal of all sockets caused differences greater than 20% in cap displacement. Apparently, CS sockets support the distribution of distal strain to more proximal CS, while collars alter CS displacement more locally. Harder sockets can increase or decrease CS displacement depending on sensor location. Furthermore, high-resolution imaging revealed that sockets are interconnected in subcuticular rows. In summary, the sensitivity of individual CS is dependent on the configuration of other CS and their substructures.

Sensory signals of unloading in insects are tuned to distinguish leg slipping from load variations in gait: experimental and modeling studies

“…Similar tests in cockroaches showed that indentation of proximal or distal tibial receptors ( Fig. 1 C , right ) did not produce spikes in other receptors, despite their close proximity ( 35 , 36 ). In contrast, reciprocal firing of the subgroups occurred when bending forces were applied to the tibia ( Fig.…”

Mechanical modeling of mechanosensitive insect strain sensors as a tool to investigate exoskeletal interfaces

“…The Journal of Comparative Neurology published by Wiley Periodicals LLC. CC BY-NC 4.0; (B) schematics of a circular and elliptical CS; there are no shorter axes in the circular CS, thus all forces from any direction can lead to compression along all axes; in elliptical CS the shorter axes is more sensitive towards compression then the longer axes; this leads to directional sensitivity through the orientation of the ellipse; (Bi) schematic showing the effects of range fractionation; the smaller the ellipse the less force is needed to lead to short axes compression; (C) schematic of a simplified CS setup based off of Grünert and Gnatzy [28], Moran et al [29], and Dinges et al [30]; L, layer; (C1) image of the 3D resin-printed model made out of three different resins; arrows indicate which aspects of the CS schematic are replicated. in turn, create varying directional stresses within the exoskeleton, which can lead to physical deformations.…”

“…Variations in cap size allows range fractionation, in which the strain magnitude is encoded within the limited sensitivity ranges of each individual cap, with the activity of the entire field encoding a broad range of strains [52,53]. Once a responseevoking strain reaches a cap, the cap displaces laterally through compression forces [29][30][31][34][35][36]. This movement can activate mechanosensitive ion channels in the CS neuron's modified dendrite [31,36,54], ultimately allowing the cuticular strain to be encoded with nanometer-scale sensitivity [41,55,56].…”

“…The resisted forces of the depressor muscle, which presses the leg and, thus, the femur against the ground during walking and jumping, should lead to dorsal bending of the femur, which should place the area of the femoral CS field (proximal ventral femur) under tension (figure 1(Ai)). Recent finite element analysis (FEA) of the femoral field also concluded that tensile displacement of the field could displace caps, with a predominant effect on more distal CS [30]. In addition, this field includes 8 elliptical CS, which should be directionally sensitive to torques because of the orientations of their long axes [44], as well as three circular CS, which should undergo strain amplification through their less-compliant collars [30,35].…”

Adaptive load feedback robustly signals force dynamics in robotic model of Carausius morosus stepping

“…In the present study, we are interested in measuring the minute strain of the leg segments as the leg steps, but to reduce runtime, multi-body physics simulators almost always model segments as “rigid bodies” that cannot bend. Computational modeling techniques such as Finite Element Analysis (FEA) are extremely useful for predicting how complex shapes such as insect leg segments would strain when stressed and have yielded valuable insights into how insects detect strain ( Kaliyamoorthy et al, 2001 ; Wang et al, 2014 , 2019 ; Noda et al, 2018 ; Dinges et al, 2022 ). However, determining and applying a realistic stress profile to the model is a challenging problem, which a robotic model inherently solves.…”